The role of poultry in the influenza ecosystem in China

Abstract

Waterfowl are regarded as the major reservoirs of influenza A virus, which maintain their diversity and provide the source of infection to other hosts. Economic development over the past three decades has greatly increased the populations and types of poultry in China, which resulted in changes of the ecology and evolutionary dynamics of influenza viruses, and the long-term enzootic status of the Asian highly pathogenic H5N1, two H9N2 and other virus lineages in the region. More recently, novel H7N9 and H10N8 viruses emerged and caused sporadic human infections, further highlighting that the current influenza ecosystem in China has posed continual threats to public health.

Using the systematic surveillance conducted on migratory birds, and domestic ducks at farms and live-poultry markets in seven provinces of southern China since 2000, potential changes in the evolutionary patterns of influenza viruses in domestic ducks and their role in the influenza ecosystem in China were investigated by considering the most commonly detected H3, H4 and H6 subtypes as representatives. Furthermore, the origin, prevalence and development of the H10N8 viruses were examined to explore the factors that are responsible for generation of novel influenza viruses in China.

A total of 276 H3 and 161 H4 duck viruses isolated in Hong Kong (1976-1981) and southern China (2000-2006) were sequenced. Phylogenetic analysis in parallel with the previously published H6 viruses revealed that domestic duck viruses from costal region of southern China and South Korea diverged from the contemporary virus gene pool, and developed into locally persistent sub-lineages. Most of domestic duck viruses in inland provinces of southern China showed extensive reassortments, maintaining viral diversity in the poultry system. An elevated evolutionary rate was observed in recent virus sub-lineages (1990 onwards) in domestic ducks compared to those from early years (1970-1980s) and from wild ducks by molecular clock analysis. This elevation is not driven by positive selection, but was likely attributed to increased number of virus replication cycles in the much larger and denser domestic duck populations.

The fourteen-year surveillance showed that H10 influenza viruses were only prevalent in ducks in Jiangxi province until it was first detected in chickens at live-poultry markets since August 2013. Phylogenetic analysis revealed that H10 viruses were regularly introduced by migratory ducks to domestic ducks on Poyang Lake. The viruses were maintained and amplified in domestic ducks and later passed to chickens at live-poultry markets, where they reassorted with enzootic H9N2 viruses to generate novel H10N8 viruses. This mirrored the pattern observed in the H7N9 outbreak and provided direct evidence of the pathway of a virus emerging from its natural reservoir to infect humans.

This thesis showed that evolution of influenza viruses in domestic ducks was influenced by contemporary poultry farming and live-poultry market system. The emergence of the H10N8 virus further highlighted the central role of domestic ducks as the major source to facilitate emergence and generation of novel subtypes of influenza viruses in the current influenza ecosystem in China.